Imagine you are floating in the dark. The only sound you can hear is that of your own breath. The temperature of the water that surrounds you is the same as that of your skin. Would you be able to tell if you have been there for five minutes or 15? The answer is no. In fact, people report that one of their first experiences in a sensory deprivation tank is losing a sense of time. Why is that?

“Time is change”, says Joe Paton, a young principal investigator at the Champalimaud Centre for the Unknown who studies how the brain generates an internal perception of time. “And even though it is a fundamental property of reality, it cannot be measured independently, it is always measured as a change in something. And in a sensory deprivation tank there is little change.”

Paton has been studying how timing information is generated in the brain since he joined the Champalimaud Foundation in 2008. During this period, he and his team have made great strides in capturing key elements of the process, including the identification of a set of neurons that can directly alter an individual’s subjective perception of time. Most recently, on May 2017, he received a prestigious International Research Scholars Program grant to support his work.

It was Paton’s fascination with the neural mechanisms of learning that led him to focus on studying how timing is represented in the brain. “In order to learn”, he explains, “the brain needs to make a mental connection between events that are separate in time. For example, a child cries and then his mother appears. It doesn’t take very long until children learn to use crying to get their parents’ attention.”

How is the brain able to create these mental connections? When trying to answer this question, one clear obstacle comes to mind: the activity of single neurons is extremely brief, lasting only a few milliseconds, but the brain has to use it to track durations which are orders of magnitude longer, from seconds, to minutes, even hours. How does it achieve that?

An ingenious code

To answer this question, together with his team, Paton chose to focus on collection of brain areas called the basal ganglia. “The basal ganglia are known to be involved in motor learning and execution of movements, both of which require timing information.” he explains. “In addition, it is known that certain neural disorders that affect the basal ganglia, such as Parkinson’s Disease, result in peculiar timing deficits in patients, which in some cases exhibit underestimation of time and in others overestimation.”

The researchers recorded multiple neurons in the basal ganglia of rats while the animals were performing a simple timing task. In this task, the animal had to report whether two brief tones were separated by an interval longer or shorter than 1.5 seconds. Results were published in 2015, showing that the neurons worked together to produce a “population clock” that timed the animals’ behaviour (Current Biology article, eLife article).

“By analysing the activity of the neurons, we found that it could be used to encode time. Specifically, we found that the first tone would evoke a wave-like pattern of activity in the neurons. Throughout this wave, certain neurons would always be active earlier and others later. In this way, we could tell how much time had passed by simply following the progression of the wave.”

This observation answered the first question, which is how the brief activity of neurons can encode long durations. But how could they confirm that the rats actually used this clock to estimate time? “We achieved that by looking at what happened to the sequences of neural activity when the animal made mistakes. For example, if the rat misjudged a short duration for a long one, we expected to see the sequence advance faster, making neurons that would usually be active later become activated earlier.”

That was precisely what they had observed. “It is as if the population clock stretched or shrunk in accordance with time as perceived by the animal.” Paton says as his arm traces an imaginary wave, “when the sequence moved too fast, the rat would mistake the duration for long and when it moved too slow, it would think it was short”.

Neurons that can make time stand still

This observation not only confirmed Paton’s hypothesis, but it also hinted at an important insight: the way animals experience time is subjective. For humans this is an unarguable fact. We all know that when we are bored time seems to pass more slowly than when we are having fun, but this data opened the door for a mechanistic exploration of this uniquely internal psychological phenomenon.

Together with his team, Paton stepped through the door. In 2016, they published a study in the journal Science revealing, for the first time, a set of neurons that directly controlled subjective time perception.

These neurons, located in an area within the basal ganglia, appeared to play a key role in time estimation. “We found not only that the activity of a group of dopamine neurons in the basal ganglia was correlated with subjective time perception in rodents, but also that selective activation of these neurons was sufficient to cause changes in the animals’ judgment of time.”

For Paton, this series of pivotal findings is only the starting point. His long-term goal is to dissect the mechanisms by which internally generated signals, such as the ones that inform the brain about the passage of time, are transformed into action.

“What is remarkable about time perception”, he points out, “is that it is a fully inward process. Just like our train of thought, it begins with a change. Something happens that suddenly sparks a flow of activity across networks of neurons that is then maintained independently of the outside world. We are used to consider these internal processes as exclusively human, but our experiments present us with a unique opportunity to pin down the neural dynamics of thought – one of our most elusive and abstract cognitive processes”.

Liad Hollender works as a Science Writer at the Science Communication Office at Champalimaud Research